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Diversity of rhizobia, symbiotic effectiveness, and potential of inoculation in Acacia mearnsii seedling production

  • Soil and Agricultural Microbiology - Research Paper
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Abstract

Black wattle (Acacia mearnsii) is a forest species of significant economic importance in southern Brazil; as a legume, it forms symbiotic associations with rhizobia, fixing atmospheric nitrogen. Nonetheless, little is known about native rhizobia in soils where the species is cultivated. Therefore, this study aimed to evaluate the diversity and symbiotic efficiency of rhizobia nodulating A. mearnsii in commercial planting areas and validate the efficiency of a potential strain in promoting seedling development. To this end, nodules were collected from four A. mearnsii commercial plantations located in Rio Grande do Sul State, southern Brazil. A total of 80 rhizobia isolates were obtained from black wattle nodules, and thirteen clusters were obtained by rep-PCR. Higher genetic diversity was found within the rhizobial populations from the Duas Figueiras (H′ = 2.224) and Seival (H′ = 2.112) plantations. Twelve isolates were evaluated belonging to the genus Bradyrhizobium, especially to the species Bradyrhizobium guangdongense. The principal component analysis indicated an association between rhizobia diversity and the content of clay, Ca, Mg, and K. Isolates and reference strains (SEMIA 6163 and 6164) induced nodulation and fixed N via symbiosis with black wattle plants after 60 days of germination. The isolates DF2.4, DF2.3, DF3.3, SEMIA 6164, SEMIA 6163, CA4.3, OV3.4, and OV1.4 showed shoot nitrogen accumulation values similar to the N + control treatment. In the second experiment (under nursery conditions), inoculation with the reference strain SEMIA 6164 generally improved the growth of A. mearnsii seedlings, reinforcing its efficiency even under production conditions.

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References

  1. Azani N, Babineau M, Bailey CD, Banks H, Barbosa AR, Pinto RB, ... Zimmerman E (2017) A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny: the Legume Phylogeny Working Group (LPWG). Taxon 66:44–77. https://doi.org/10.12705/661.3

  2. Taylor DB, Dhileepan K (2019) Implications of the changing phylogenetic relationships of Acacia sl on the biological control of Vachellia nilotica ssp. indica in Australia. Ann Appl Biol 174:238–247. https://doi.org/10.1111/aab.12499

    Article  Google Scholar 

  3. Griffin AR, Midgley SJ, Bush D, Cunningham PJ, Rinaudo AT (2011) Global uses of Australian acacias—recent trends and future prospects. Divers Distrib 17:837–847. https://doi.org/10.1111/j.1472-4642.2011.00814.x

    Article  Google Scholar 

  4. Simon AA, São José JFB, Behling M (2013) Sustentabilidade da produção de madeira e de casca de Acácia Negra. In: Silva LD, Higa AR (ed) Sustentabilidade de Sistemas de Produção Florestal, 1ed. Curitiba, FUPEF, pp. 315–360.

  5. AGEFLOR—Associação Gaúcha De Empresas Florestais. A Indústria de base florestal no Rio Grande do Sul (2020) Report 2020. Porto Alegre, Brazil. https://www.ageflor.com.br/noticias/wp-content/uploads/2020/12/O-Setor-de-Base-Florestal-no-Rio-Grande-do-Sul-2020-ano-base-2019.pdf. Accessed 08 February 2021

  6. Schumacher MV, Brum EJ, Rodrigues LM, Santos EM (2003) Nutrient return via litter deposition in a black wattle (Acacia mearnsii De Wild.) stand in Rio Grande do Sul. Brazil J Braz For Sci 27:79–798. https://doi.org/10.1590/S0100-67622003000600005

    Article  Google Scholar 

  7. Forrester DI, Pares A, O’Hara C, Khanna PK, Bauhus J (2013) Soil organic carbon is increased in mixed-species plantations of eucalyptus and nitrogen-fixing acacia. Ecosystems 16:123–132. https://doi.org/10.1007/s10021-012-9600-9

    Article  CAS  Google Scholar 

  8. de Godoi SG, Neufeld ADH, Ibarr MA, Ferreto DOC, Bayer C, Lorentz LH, Vieira FCB (2016) The conversion of grassland to acacia forest as an effective option for net reduction in greenhouse gas emissions. J Environ Manag 169:91–102. https://doi.org/10.1016/j.jenvman.2015.11.057

    Article  CAS  Google Scholar 

  9. Lafay B, Burdon JJ (2001) Small-subunit rRNA genotyping of rhizobia nodulating Australian acacia spp. Appl Environ Microbiol 67:396–402. https://doi.org/10.1128/aem.67.1.396-402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ngom A, Nakagawa Y, Sawada H, Tsukahara J, Wakabayashi S, Uchiumi T, Nuntagij A, Kotepong S, Suzuki A, Higashi S, Abe M (2004) A novel symbiotic nitrogen-fixing member of the Ochrobactrum clade isolated from root nodules of Acacia mangium. J Gen Appl Microbiol 50:17–27. https://doi.org/10.2323/jgam.50.17

    Article  CAS  PubMed  Google Scholar 

  11. Monteiro PHR, Kaschuk G, Winagraski E, Auer CG, Higa AR (2019) Rhizobial inoculation in black wattle plantation (Acacia mearnsii De Wild.) in production systems of southern Brazil. Braz J Microbiol 50:989–998. https://doi.org/10.1007/s42770-019-00148-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Menna P, Hungria M, Barcellos FG, Bangel EV, Hess PN, Martínez-Romero E (2006) Molecular phylogeny based on the 16S rRNA gene of elite rhizobial strains used in Brazilian commercial inoculants. Syst Appl Microbiol 29:315–332. https://doi.org/10.1016/j.syapm.2005.12.002

    Article  CAS  PubMed  Google Scholar 

  13. Rodríguez-Echeverría S, Le Roux JJ, Crisóstomo JA, Ndlovu J (2011) Jack-of-all-trades and master of many? How does associated rhizobial diversity influence the colonization success of Australian Acacia species? Divers Distrib 17:946–957. https://doi.org/10.1111/j.1472-4642.2011.00787.x

    Article  Google Scholar 

  14. Vargas LK, Lisboa BB, Scholles D, Silveira JRP, Jung GC, Granada CE, Neves AG, Braga MM, Negreiros T (2007) Genetic diversity and symbiotic efficiency of black wattle-nodulating rhizobia in soils of Rio Grande do Sul State, Brazil. Braz J Soil Sci 31:647–654

    CAS  Google Scholar 

  15. Salto CS, Melchiorre M, Oberschelp GPJ, Pozzi E, Harrand L (2019) Effect of fertilization and inoculation with native rhizobial strains on growth of Prosopis alba seedlings under nursery conditions. Agrofor Syst 93:621–629. https://doi.org/10.1007/s10457-017-0156-8

    Article  Google Scholar 

  16. Sutherland JM, Odee DW, Muluvi GM, McInroy SGA (2000) Patel Single and multi-strain rhizobial inoculation of African Acacias in nursery conditions. Soil Biol Biochem 32:323–333. https://doi.org/10.1016/S0038-0717(99)00157-1

    Article  CAS  Google Scholar 

  17. Sarr A, Diop B, Peltier R, Neyra M, Lesueur D (2005) Effect of rhizobial inoculation methods and host plant provenances on nodulation and growth of Acacia senegal and Acacia nilotica. New For 29:75–87. https://doi.org/10.1007/s11056-004-5232-z

    Article  Google Scholar 

  18. Sarr A, Lesueur D (2006) Influence of soil fertility on the rhizobial competitiveness for nodulation of Acacia senegal and Acacia nilotica provenances in nursery and field conditions. World J Microbiol Biotechnol 23:705–711. https://doi.org/10.1007/s11274-006-9288-0

    Article  Google Scholar 

  19. Galiana A, Chaumont J, Diem HG, Dommergues YR (1990) Nitrogen-fixing potential of Acacia mangium and Acacia auriculiformis seedlings inoculated with Bradyrhizobium and Rhizobium spp. Biol Fertil Soils 9:261–267. https://doi.org/10.1007/BF00336237

    Article  Google Scholar 

  20. Jayakumar P, Tan TK (2006) Variations in the responses of Acacia mangium to inoculation with different strains of Bradyrhizobium sp. under nursery conditions. Symbiosis 41:31–37

    Google Scholar 

  21. Brasil (2011) SDA/MAPA Normative Instruction nº 13/2011. http://www.agricultura.gov.br/assuntos/insumos-agropecuarios/insumos-agricolas/fertilizantes/legislacao/in-sda–13-de–24–03–2011-inoculantes.pdf Accessed 08 February 2021

  22. São José JFB, Volpiano CG, Vargas LK, Hernandes MAS, Lisboa BB, Schlindwein G, Sampaio JAT, Beneduzi A, Longoni LS (2019) Influence of hot water on breaking dormancy, incubation temperature and rhizobial inoculation on germination of Acacia mearnsii seeds. Aust For 1:1–5. https://doi.org/10.1080/00049158.2019.1636350

    Article  Google Scholar 

  23. Karthikeyan A, Arunprasad T (2019) Growth response of Pterocarpus santalinus seedlings to native microbial symbionts (arbuscular mycorrhizal fungi and Rhizobium aegyptiacum) under nursery conditions. J For Res 32:225–231. https://doi.org/10.1007/s11676-019-01072-y

    Article  CAS  Google Scholar 

  24. Brockwell J, Mitchell PA, Searle SD, Leach MA, Crews TE (2011) Direct benefits of rhizobial inoculation to Acacia mearnsii De Wild, as tubed stock and in a plantation, and synergistic benefits to interplanted Eucalyptus nitens (Deane & Maiden) Maiden. Aust For 74:120–132. https://doi.org/10.1080/00049158.2011.10676354

    Article  Google Scholar 

  25. Kaur A, Chaukiyal SP, Thakur A, Pokhriyal TC (2013) Effect of rhizobial inoculations on nitrogen metabolism of Albizia lebbek seedlings. J For Res 24:671–676. https://doi.org/10.1007/s11676-013-0403-4

    Article  CAS  Google Scholar 

  26. Vincent JM (1970) A manual for the practical study of root nodule-bacteria. Oxford-Edinburgh: Blackwell Scientific. https://doi.org/10.1002/jobm.19720120524

  27. Tedesco MJ, Gianello C, Bissani CA, Bohnen H, Volkweiss SJ (1995) Análise de solo, plantas e outros materiais (Boletim Técnico de Solos, 5). Departamento de Solos, UFRGS, Porto Alegre

  28. Sambrook J, Russel D (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

  29. Wright ES (2015) DECIPHER: harnessing local sequence context to improve protein multiple sequence alignment. BCM Bioinformatics 16:322. https://doi.org/10.1186/s12859-015-0749-z

    Article  CAS  Google Scholar 

  30. Schliep KP (2011) Phangorn: phylogenetic analysis in R. Bioinformatics 27:592–593. https://doi.org/10.1093/bioinformatics/btq706

    Article  CAS  PubMed  Google Scholar 

  31. Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x

    Article  Google Scholar 

  32. Yu G, Smith DK, Zhu H, Guan Y, Lam TTY (2017) Ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 8:28–36. https://doi.org/10.1111/2041-210X.12628

    Article  Google Scholar 

  33. Asghar HN, Zahir ZA, Arshad M, Khaliq A (2002) Relationship between in vitro production of auxins by rhizobacteria and their growth-promoting activities in Brassica juncea L. Biol Fertil Soils 35:231–237. https://doi.org/10.1007/s00374-002-0462-8

    Article  CAS  Google Scholar 

  34. Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Champaign

    Google Scholar 

  35. Borges LGDA, Dalla Vechia V, Corção G (2003) Characterization and genetic diversity via REP-PCR of Escherichia coli isolates from polluted waters in southern Brazil. FEMS Microbiol Ecol 45:173–180. https://doi.org/10.1016/s0168-6496(03)00147-8

    Article  Google Scholar 

  36. Kaschuk G, Hungria M, Andrade DS, Campo RJ (2006) Genetic diversity of rhizobia associated with common bean (Phaseolus vulgaris L.) grown under no-tillage and conventional systems in Southern Brazil. Appl Soil Ecol 32:210–220. https://doi.org/10.1016/j.apsoil.2005.06.008

    Article  Google Scholar 

  37. Rico A, Ortiz-Barredo A, Ritter E, Murillo J (2004) Genetic characterization of Erwinia amylovora strains by amplified fragment length polymorphism. J Appl Microbiol 96:302–310. https://doi.org/10.1046/j.1365-2672.2003.02156.x

    Article  CAS  PubMed  Google Scholar 

  38. Rohlf FJ (1990) NTSYS-pc numerical taxonomy and multivariate system. Version 2.01. Exeter Software. New York: Setauket.

  39. Hammer O, Harper DAT, Ryan PD (2007) PAST: palentological statistics software for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  40. Dickson A, Leaf AL, Hosner JF (1960) Quality appraisal of white spruce and white pine seedling stock in nurseries. For Chron 36:10–13. https://doi.org/10.5558/tfc36010-1

    Article  Google Scholar 

  41. Ferreira DF (2011) Sisvar: a computer statistical analysis system. Cienc Agrotec 35:1039–1042. https://doi.org/10.1590/S1413-70542011000600001

    Article  Google Scholar 

  42. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer K, Whitman WB, Euzéby J, Amann R, Móra RR (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645. https://doi.org/10.1038/nrmicro3330

    Article  CAS  PubMed  Google Scholar 

  43. Li YH, Wang R, Zhang XX, Young JPW, Wang ET, Sui XH, Chen W, Chen WX (2015) Bradyrhizobium guangdongense sp. nov. and Bradyrhizobium guangxiense sp. nov., isolated from effective nodules of peanut. Int J Syst Evol Microbiol 65:4655–4661. https://doi.org/10.1099/ijsem.0.000629

    Article  CAS  PubMed  Google Scholar 

  44. Zhang J, Peng S, Li S, Song J, Brunel B, Wang E, James EK, Chen W, Andrews M (2021) Arachis hypogaea L. from acid soils of Nanyang (China) is frequently associated with Bradyrhizobium guangdongense and occasionally with Bradyrhizobium ottawaense or three Bradyrhizobium genospecies. Microb Ecol:1–9. https://doi.org/10.1007/s00248-021-01852-2

  45. Chahboune R, Carro L, Peix A, Ramírez-Bahena MH, Barrijal S, Velázquez E, Bedmar EJ (2012) Bradyrhizobium rifense sp. nov. isolated from effective nodules of Cytisus villosus grown in the Moroccan Rif. Syst Appl Microbiol 35:302–305. https://doi.org/10.1016/j.syapm.2012.06.001

    Article  CAS  PubMed  Google Scholar 

  46. Lu JK, Dou YJ, Zhu YJ, Wang SK, Sui XH, Kang LH (2014) Bradyrhizobium ganzhouense sp. nov., an effective symbiotic bacterium isolated from Acacia melanoxylon R. Br. nodules. Int J Syst Evol Microbiol 64:1900–1905. https://doi.org/10.1099/ijs.0.056564-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Li YH, Wang R, Sui XH, Wang ET, Zhang XX, Tian CF, Chen WF, Chen WX (2019) Bradyrhizobium nanningense sp. nov., Bradyrhizobium guangzhouense sp. nov. and Bradyrhizobium zhanjiangense sp. nov., isolated from effective nodules of peanut in Southeast China. Syst Appl Microbiol 42:126002. https://doi.org/10.1016/j.syapm.2019.126002

  48. Banasiewicz J, Lisboa BB, Da Costa PB, Schlindwein G, Venter SN, Steenkamp ET, Vargas LK, Passaglia LMP, Stępkowski T (2021) Culture-independent assessment of the diazotrophic Bradyrhizobium communities in the Pampa and Atlantic Forest Biomes localities in southern Brazil. Syst Appl Microbiol 44:126228. https://doi.org/10.1016/j.syapm.2021.126228

    Article  PubMed  Google Scholar 

  49. Volpiano CG, Santanna F, Ambrosini A, São José JFB, Beneduzi A, Whitman WB, Souza EM, Lisboa BB, Vargas LK, Passaglia LMP (2021) Genomic metrics applied to Rhizobiales (Hyphomicrobiales): species reclassification, identification of unauthentic genomes and false type strains. Front Microbiol 12:614957. https://doi.org/10.3389/fmicb.2021.614957

    Article  PubMed  PubMed Central  Google Scholar 

  50. Klenk HP, Göker M (2010) En route to a genome-based classification of Archaea and Bacteria? Syst Appl Microbiol 33:175–182. https://doi.org/10.1016/j.syapm.2010.03.003

    Article  CAS  PubMed  Google Scholar 

  51. Ali B, Hayat S, Aiman Hasan S, Ahmad A (2008) A comparative effect of IAA and 4-Cl-IAA on growth, nodulation and nitrogen fixation in Vigna radiata (L.) Wilczek. Acta Physiol Plant 30:35–41. https://doi.org/10.1007/s11738-007-0088-4

    Article  CAS  Google Scholar 

  52. Tullio LD, Nakatani AS, Gomes DF, Ollero FJ, Megías M, Hungria M (2019) Revealing the roles of y4wF and tidC genes in Rhizobium tropici CIAT 899: biosynthesis of indolic compounds and impact on symbiotic properties. Arch Microbiol 201:171–183. https://doi.org/10.1007/s00203-018-1607-y

    Article  CAS  PubMed  Google Scholar 

  53. Kumar V, Rawat AK, Rao DLN (2017) Population ecology of soybean-rhizobia in diverse crop rotations in Central India. Agr Ecosyst Environ 240:261–268. https://doi.org/10.1016/j.agee.2017.02.011

    Article  Google Scholar 

  54. Castro-Pires R, Reis-Junior FB, Zilli JE, Fischer D, Hofmann A, James EK, Simon MF (2018) Soil characteristics determine the rhizobia in association with different species of Mimosa in central Brazil. Plant Soil 423:411–428. https://doi.org/10.1007/s11104-017-3521-5

    Article  CAS  Google Scholar 

  55. Lindström K, Mousavi SA (2019) Effectiveness of nitrogen fixation in rhizobia. Microb Biotechnol 13:1314–1335. https://doi.org/10.1111/1751-7915.13517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Cao Y, Wang ET, Zhao L, Chen WM, Wei GH (2014) Diversity and distribution of rhizobia nodulated with Phaseolus vulgaris in two ecoregions of China. Soil Biol Biochem 78:128–137. https://doi.org/10.1016/j.soilbio.2014.07.026

    Article  CAS  Google Scholar 

  57. Wang L, Cao Y, Wang ET, Qiao YJ, Jiao S, Liu ZS, Zhao L, Wei GH (2016) Biodiversity and biogeography of rhizobia associated with common bean (Phaseolus vulgaris L.) in Shaanxi province. Syst Appl Microbiol 39:211–219. https://doi.org/10.1016/j.syapm.2016.02.001

    Article  PubMed  Google Scholar 

  58. Wu YC, Zeng J, Zhu Q, Zhang Z, Lin X (2017) PH is the primary determinant of the bacterial community structure in agricultural soils impacted by polycyclic aromatic hydrocarbon pollution. Sci Rep 7:1–7. https://doi.org/10.1038/srep40093

    Article  CAS  Google Scholar 

  59. Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989. https://doi.org/10.1128/MMBR.63.4.968-989.1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Yang SS, Bellogín RA, Buendía A, Camacho M, Chen M, Cubo T, Daza A, Díaz CL, Espuny MR, Gutiérrez R, Harteveld M, Li XH, Lyra MCCP, Madinabeitia N, Medina C, Miao L, Ollero FJ, Olsthoorn MMA, Rodríguez DN, Santamaría C, Schlaman HRM, Spaink HP, Temprano F, Thomas-Oates JE, Van Brussel AAN, Vinardell JM, Xie F, Yang J, Zhang HY, Zhen J, Zhou J, Ruiz-Sainz JE (2001) Effect of pH and soybean cultivars on the quantitative analyses of soybean rhizobia populations. J Biotechnol 91:243–255. https://doi.org/10.1016/S0168-1656(01)00340-6

    Article  CAS  PubMed  Google Scholar 

  61. Andrade DS, Murphy PJ, Giller KE (2002) The diversity of Phaseolus-nodulating rhizobial populations is altered by liming of acid soils planted with Phaseolus vulgaris L. in Brazil. Appl Environ Microbiol 68:4025–4034. https://doi.org/10.1128/aem.68.8.4025-4034.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Giongo A, Ambrosini A, Vargas LK, Freire JRJ, Bodanese-Zanettini MH, Passaglia LMP (2008) Evaluation of genetic diversity of bradyrhizobia strains nodulating soybean Glycine max (L.) Merrill. isolated from South Brazilian fields. Appl Soil Ecol 38:261–269. https://doi.org/10.1016/j.apsoil.2007.10.016

    Article  Google Scholar 

  63. Liu L, Chen X, Hu S (2021) Genetic diversity and distribution of rhizobia associated with soybean in red soil in Hunan Province. Arch Microbiol 203:1971–1980. https://doi.org/10.1007/s00203-020-02120-6

    Article  CAS  PubMed  Google Scholar 

  64. Coutinho HLC, Oliveira VM, Lovato A, Maia AHN, Manfio GP (1999) Evaluation of the diversity of rhizobia in Brazilian agricultural soils cultivated with soybeans. Appl Soil Ecol 13:159–167. https://doi.org/10.1016/S0929-1393(99)00031-1

    Article  Google Scholar 

  65. Zilli JÉ, Valisheski RR, Freire Filho FR, Prata Neves MC, Rumjanek NG (2004) Assessment of cowpea Rhizobium diversity in Cerrado areas of northeastern Brazil. J Microb 35:281–287. https://doi.org/10.1590/S1517-83822004000300002

    Article  Google Scholar 

  66. Ngo Nkot L, Krasova-Wade T, Etoa FX, Sylla SN, Nwaga D (2008) Genetic diversity of rhizobia nodulating Arachis hypogaea L. in diverse land use systems of humid forest zone in Cameroon. Appl Soil Ecol 40:411–416. https://doi.org/10.1016/j.apsoil.2008.06.007

    Article  Google Scholar 

  67. Shao S, Chen M, Liu W, Hu X, Wang ET, Yu S, Li Y (2020) Long-term monoculture reduces the symbiotic rhizobial biodiversity of peanut. Syst Appl Microbiol 43:126101. https://doi.org/10.1016/j.syapm.2020.126101

    Article  CAS  PubMed  Google Scholar 

  68. Yan J, Han XZ, Chen X, Lu XC, Chen WF, Wang ET, Zou WX, Zhang ZM (2019) Effects of long-term fertilization strategies on soil productivity and soybean rhizobial diversity in a Chinese Mollisol. Pedosphere 29:784–793. https://doi.org/10.1016/S1002-0160(17)60470-3

    Article  CAS  Google Scholar 

  69. Vargas LK, Volpiano CG, Lisboa BB, Giongo A, Beneduzi A, Passaglia LMP (2017) Potential of rhizobia as plant growth–promoting rhizobacteria. In: Khan MS, Zaide A, Musarrat J (eds) Microbes for legume improvement. Springer, Berlin, pp.153–174. https://doi.org/10.1007/978-3-319-59174-2_7

  70. Sutherland J (2000) Single and multi-strain rhizobial inoculation of African acacias in nursery conditions. Soil Biol Biochem 32:323–333. https://doi.org/10.1016/S0038-0717(99)00157-1

    Article  CAS  Google Scholar 

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Funding

This work was financed by a grant and fellowships from the Fundação de Amparo à Pesquisa do Estado Do Rio Grande do Sul (Fapergs/Brazil) and Fundo Estadual de Desenvolvimento Florestal- FUNDEFLOR (SEAPDR/Brazil).

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  1. Department of Agricultural Research and Diagnosis - DDPA, Secretary of Agriculture, Livestock, and Rural Development of Rio Grande do Sul - SEAPDR, 570 Gonçalves Dias St, 90130-060, Porto Alegre, Rio Grande do Sul, Brazil

    Jackson Freitas Brilhante de São José, Bruno Brito Lisboa, Anelise Beneduzi & Luciano Kayser Vargas

  2. La Salle University - Unilasalle, 2288 Vitor Barreto Ave, 92010-000, Canoas, Rio Grande do Sul, Brazil

    Marcos André Santos Hernandes

  3. Department of Genetics, Universidade Federal do Rio Grande do Sul - UFRGS, 9500 Bento Gonçalves Ave, 91501-970, Porto Alegre, Rio Grande do Sul, Brazil

    Camila Gazolla Volpiano & Luciane Maria Pereira Passaglia

  4. Department of Soil Science, Faculty of Agronomy, Universidade Federal do Rio Grande do Sul - UFRGS, 7712 Bento Gonçalves Ave, 91540-000, Porto Alegre, Rio Grande do Sul, Brazil

    Cimelio Bayer

  5. Tanagro S/A, 199 Torbjorn Weibull St, 95780-000, Montenegro, Rio Grande do Sul, Brazil

    Augusto Arlindo Simon & Jeferson de Oliveira

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  1. Jackson Freitas Brilhante de São José
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Contributions

Material and methods preparation, and analysis were performed by JFBSJ, MASH, CGV, CB, and BBL. AAS and JO performed field collections and logistical support. Grant and fellowships acquisition were provided by JFBSJ, LMPP, and AB. The manuscript was written by LKV, JFBSJ, and AB. All authors commented on previous versions of the manuscript and approved the final manuscript.

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Correspondence to Anelise Beneduzi.

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de São José, J.F.B., Hernandes, M.A.S., Volpiano, C.G. et al. Diversity of rhizobia, symbiotic effectiveness, and potential of inoculation in Acacia mearnsii seedling production. Braz J Microbiol 54, 335–348 (2023). https://doi.org/10.1007/s42770-022-00867-2

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  • DOI: https://doi.org/10.1007/s42770-022-00867-2

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